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Adenovirus E1A: remodelling the host cell, a life or death experience

Oncogene volume 20, pages 7824–7835 (2001)Cite this article

It came as a considerable surprise to virologists in 1962 when John Trentin and his colleagues (Trentin et al., 1962) reported that a human adenovirus was oncogenic. At Baylor University (Houston, Texas) they had been inoculating newborn hamsters with human adenoviruses and found that adenovirus serotype 12 (Ad12) induced tumours in a high proportion of the animals injected. Other Ad serotypes (Ads) were found to be non-tumorigenic (this included Ad2, which with its closely related non-oncogenic serotype Ad5, have been the most extensively studied Ads; referred to in this review as Ad2/5). This important observation was initially greeted with some scepticism (see Gross, 1996). However, Ad12 oncogenesis was rapidly confirmed by others (Huebner et al., 1962) and lead to more extensive in vivo and in vitro studies on the capacity of human Ads to disrupt normal cell growth control. It is not possible to review all of the literature on this subject here but there are a number of reviews that cover this subject (Gross, 1996; Gallimore et al., 1984; Williams et al., 1995). From the in vivo studies in the 1960's it soon became clear that there were indeed tumorigenic (Huebner et al., 1962; Trentin et al., 1962, Girardi et al., 1964; Pereira et al., 1965) and non-tumorigenic adenoviruses (Trentin et al., 1962, 1968). As well as Ad serotype, adenovirus induced tumorigenicity was found to be dependent on virus dose (Yabe et al., 1962), host genetic constitution (Yabe et al., 1964, Yohn et al., 1965; Allison et al., 1967), age at inoculation (Yabe et al., 1962) and the host's immune status (Yohn et al., 1965; Allison et al., 1967). Around this time tissue culture studies revealed that rodent cells were susceptible to adenovirus transformation and that both tumorigenic (McBride and Wiener, 1964) and non-tumorigenic Ads (Freeman et al., 1967) induced morphological transformation from which immortal cell lines could be easily derived. Studies on immortal rodent cell lines showed that the cells transformed by non-oncogenic viruses could be tumorigenic, but only in immunocompromised hosts (Gallimore, 1972, Gallimore et al., 1977).

The next logical step in adenovirus research was to identify the virus genes responsible for transformation and/or tumorigenicity. Unlike today, no restriction enzymes were readily available and there was no Southern blotting technique (Southern, 1975). Fujinaga and Green used membrane hybridization to show that adenovirus sequences were indeed retained and expressed in Ad transformed cells (Fujinaga and Green, 1970). This was followed by the first attempt to utilize restriction endonucleases and Cot analysis (Pettersson and Sambrook, 1973) to map the viral sequences in an Ad2 transformed line, Ad2/8617. In the following year, a more extensive study found that a minimal region of the virus genome representing the left hand 14% was common to nine independently isolated Ad2 transformed rat embryo cell lines (Gallimore et al., 1974). This strongly suggested, but did not prove, that the Ad transforming gene resided in this region of the Ad genome. With the development of the calcium phosphate DNA transfection technique (Graham and van der Eb, 1973) and the use of defined Ad DNA fragments, it was convincingly shown that this region was responsible for the induction of transformation (Graham et al., 1974a,b). RNA mapping was carried out (Sharp et al., 1974; Flint et al., 1975) which defined the early region transcripts (reviewed by Shenk and Flint, 1991; Shenk, 1996) and later designated E1 (E1A+E1B) E2, E3 and E4 (Kitchingman et al., 1977). Viral RNA selected on specific Ad DNA fragments was then used in transcription/translation assays to identify the proteins expressed from these regions and their molecular weights (Lewis et al., 1976; Harter and Lewis, 1978; Halbert et al., 1979). The E1A proteins were found to have a molecular weight range from approximately 28 to 58 kDa.

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Acknowledgements

We are extremely grateful to our colleague Roger Grand for his input to this review and to the following for their advice and rapid replies to our e-mails, Arnie Berk, Ron Hay, David Livingston and Joe Mymryk. We are extremely grateful to David Molloy for communicating unpublished data on E1A structure and Miriam Fuchs for information regarding p400. AS Turnell is funded by a Cancer Research Campaign Programme Grant SP19414/2701 and PH Gallimore is a CRC Gibb Fellow.

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Gallimore, P., Turnell, A. Adenovirus E1A: remodelling the host cell, a life or death experience. Oncogene 20, 7824–7835 (2001). https://doi.org/10.1038/sj.onc.1204913

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